Co-infection of Four Novel Mycoviruses from Three Lineages Confers Hypovirulence on Phytopathogenic Fungus Ustilaginoidea virens
Yu Fan,
Wenhua Zhao,
Xiaolin Tang,
Mei Yang,
Yingqing Yang,
Zixuan Zhang,
Baoping Cheng,
Erxun Zhou,
Zhenrui He
Affiliations
Yu Fan
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Wenhua Zhao
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Xiaolin Tang
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Mei Yang
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Yingqing Yang
Institute of Plant Protection, Jiangxi Academy of Agricultural Sciences
Zixuan Zhang
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Baoping Cheng
Institute of Plant Protection, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of High Technology for Plant Protection/Key Laboratory of Green Prevention and Control On Fruits and Vegetables in South China, Ministry of Agriculture and Rural Affairs
Erxun Zhou
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Zhenrui He
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University
Abstract Rice false smut caused by Ustilaginoidea virens has become one of the most important diseases of rice. Mycoviruses are viruses that can infect fungi with the potential to control fungal diseases. However, little is known about the biocontrol role of hypoviruses in U. virens. In this study, we revealed that the hypovirulence-associated U. virens strain Uv325 was co-infected by four novel mycoviruses from three lineages, designated Ustilaginoidea virens RNA virus 16 (UvRV16), Ustilaginoidea virens botourmiavirus virus 8 (UvBV8), Ustilaginoidea virens botourmiavirus virus 9 (UvBV9), and Ustilaginoidea virens narnavirus virus 13 (UvNV13), respectively. The U. virens strain co-infected by four mycoviruses showed slower growth rates, reduced conidial yield, and attenuated pigmentation. We demonstrated that UvRV16 was not only the major factor responsible for the hypovirulent phenotype in U. vriens, but also able to prevent U. virens to accumulate more mycotoxin, thereby weakening the inhibitory effects on rice seed germination and seedling growth. Additionally, we indicated that UvRV16 can disrupt the antiviral response of U. virens by suppressing the transcriptional expression of multiple genes involved in autophagy and RNA silencing. In conclusion, our study provided new insights into the biological control of rice false smut.